Impact of exercise training on the sarcopenia criteria in non-alcoholic fatty liver disease: a systematic review and meta-analysis

Submitted: 21 January 2021
Accepted: 7 February 2021
Published: 19 February 2021
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Sarcopenia is a highly prevalent complication of non-alcoholic fatty liver disease (NAFLD). We aimed to conduct a systematic review and meta-analyses to elucidate the exercise training (ET)'s efficacy on NAFLD adult patients' sarcopenia criteria. We identified relevant randomized controlled trials (RCT) in electronic databases PubMed, CINAHL, and Scopus. We selected seven RCT from 66 screened studies. The ET programs included endurance or combined (endurance and resistance) training. No study performed resistance training alone. The physical function improved with endurance or combined training (mean differences [MD] 8.26 mL/Kg*min [95% CI 5.27 to 11.24 mL/Kg*min], p < 0.0001); Muscle mass showed no evidence of the beneficial effects of endurance or combined training (MD 1.01 Kg [95% CI -1.78 to 3.80 Kg], p = 0.48). None of the selected studies evaluated muscle strength. Endurance and combined training increase physical function criteria but do not improve muscle mass criteria on sarcopenia in NAFLD patients. These results must be interpreted with caution for the small number of patients included in the RCTs analyzed, the different characteristics of the ET carried out, the non-use of resistance training, which prevents assess its effect on sarcopenia despite the evidence that recommends it and does not assessment muscle strength criteria in RCT include. Future research should include muscle strength assessments and resistance training to evaluate the effects in this condition. Exercise training is beneficial for sarcopenia in NAFLD but is necessary more experimental evidence to define the best type of training that positively affects the three criteria of sarcopenia. PROSPERO reference number CRD42020191471.

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El Sherif O, Dhaliwal A, Newsome PN,Armstrong MJ. Sarcopenia in nonalcoholic fatty liver disease: new challenges for clinical practice. Expert Rev Gastroenterol Hepatol 2020; 14: 197-205. DOI: https://doi.org/10.1080/17474124.2020.1731303
Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M,Sanyal AJ. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 2012; 55: 2005-23. DOI: https://doi.org/10.1002/hep.25762
Yu R, Shi Q, Liu L,Chen L. Relationship of sarcopenia with steatohepatitis and advanced liver fibrosis in non-alcoholic fatty liver disease: a meta- analysis. BMC Gastroenterol 2018; 18: 51. DOI: https://doi.org/10.1186/s12876-018-0776-0
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M, Writing Group for the European Working Group on Sarcopenia in Older P,the Extended Group for E. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48: 601. DOI: https://doi.org/10.1093/ageing/afz046
Lee YH, Jung KS, Kim SU, Yoon HJ, Yun YJ, Lee BW, Kang ES, Han KH, Lee HC,Cha BS. Sarcopaenia is associated with NAFLD independently of obesity and insulin resistance: Nationwide surveys (KNHANES 2008-2011). J Hepatol 2015; 63: 486-93. DOI: https://doi.org/10.1016/j.jhep.2015.02.051
Dasarathy S. Treatment to improve nutrition and functional capacity evaluation in liver transplant candidates. Curr Treat Options Gastroenterol 2014; 12: 242-55. DOI: https://doi.org/10.1007/s11938-014-0016-9
Meeks AC,Madill J. Sarcopenia in liver transplantation: A review. Clin Nutr ESPEN 2017; 22: 76-80. DOI: https://doi.org/10.1016/j.clnesp.2017.08.005
Tandon P, Dunn MA,Duarte-Rojo A. Resistance Training Reduces Risk of Sarcopenia in Patients With Cirrhosis. Clin Gastroenterol Hepatol 2020; 18: 1036-9. DOI: https://doi.org/10.1016/j.cgh.2019.09.030
Aamann L, Dam G, Rinnov AR, Vilstrup H,Gluud LL. Physical exercise for people with cirrhosis. Cochrane Database Syst Rev 2018; 12: CD012678. DOI: https://doi.org/10.1002/14651858.CD012678.pub2
Smart NA, King N, McFarlane JR, Graham PL,Dieberg G. Effect of exercise training on liver function in adults who are overweight or exhibit fatty liver disease: a systematic review and meta- analysis. Br J Sports Med 2018; 52: 834-43. DOI: https://doi.org/10.1136/bjsports-2016-096197
Medrano M, Cadenas-Sanchez C, Álvarez-Bueno C, Cavero-Redondo I, Ruiz JR, Ortega FB,Labayen I. Evidence-Based Exercise Recommendations to Reduce Hepatic Fat Content in Youth- a Systematic Review and Meta-Analysis. Prog Cardiovasc Dis 2018; 61: 222-31. DOI: https://doi.org/10.1016/j.pcad.2018.01.013
Guyatt GH, Oxman AD, Kunz R, Atkins D, Brozek J, Vist G, Alderson P, Glasziou P, Falck-Ytter Y ,Schunemann HJ. GRADE guidelines: 2. Framing the question and deciding on important outcomes. J Clin Epidemiol 2011; 64: 395-400. DOI: https://doi.org/10.1016/j.jclinepi.2010.09.012
Younossi ZM. Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: Implications for liver transplantation. Liver Transpl 2018; 24: 166-70. DOI: https://doi.org/10.1002/lt.25003
Perumpail BJ, Khan MA, Yoo ER, Cholankeril G, Kim D,Ahmed A. Clinical epidemiology and disease burden of nonalcoholic fatty liver disease. World J Gastroenterol 2017; 23: 8263-76. DOI: https://doi.org/10.3748/wjg.v23.i47.8263
van Deursen VM, Damman K, Hillege HL, van Beek AP, van Veldhuisen DJ,Voors AA. Abnormal liver function in relation to hemodynamic profile in heart failure patients. J. Card. Fail. 2010; 16: 84-90. DOI: https://doi.org/10.1016/j.cardfail.2009.08.002
Kong LZ, Chandimali N, Han YH, Lee DH, Kim JS, Kim SU, Kim TD, Jeong DK, Sun HN, Lee DS,Kwon T. Pathogenesis, Early Diagnosis, and Therapeutic Management of Alcoholic Liver Disease. Int J Mol Sci 2019; 20: 2712. DOI: https://doi.org/10.3390/ijms20112712
Engelking LR, Dasher CA,Hirschowitz BI. Within- day fluctuations in serum bile-acid concentrations among normal control subjects and patients with hepatic disease. Am J Clin Pathol 1980; 73: 196- 201. DOI: https://doi.org/10.1093/ajcp/73.2.196
Suchomel TJ, Nimphius S,Stone MH. The Importance of Muscular Strength in Athletic Performance. Sports Med 2016; 46: 1419-49. DOI: https://doi.org/10.1007/s40279-016-0486-0
Heymsfield SB, McManus C, Smith J, Stevens V,Nixon DW. Anthropometric measurement of muscle mass: revised equations for calculating bone-free arm muscle area. Am J Clin Nutr 1982; 36: 680-90. DOI: https://doi.org/10.1093/ajcn/36.4.680
Beaudart C, Rolland Y, Cruz-Jentoft AJ, Bauer JM, Sieber C, Cooper C, Al-Daghri N, Araujo de Carvalho I, Bautmans I, Bernabei R, Bruyere O, Cesari M, Cherubini A, Dawson-Hughes B, Kanis JA, Kaufman JM, Landi F, Maggi S, McCloskey E, Petermans J, Rodriguez Manas L, Reginster JY, Roller-Wirnsberger R, Schaap LA, Uebelhart D, Rizzoli RFielding RA. Assessment of Muscle Function and Physical Performance in Daily Clinical Practice : A position paper endorsed by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO). Calcif Tissue Int 2019; 105: 1-14. DOI: https://doi.org/10.1007/s00223-019-00545-w
Sullivan S, Kirk EP, Mittendorfer B, Patterson BW,Klein S. Randomized trial of exercise effect on intrahepatic triglyceride content and lipid kinetics in nonalcoholic fatty liver disease. Hepatology 2012; 55: 1738-45. DOI: https://doi.org/10.1002/hep.25548
Pugh CJ, Cuthbertson DJ, Sprung VS, Kemp GJ, Richardson P, Umpleby AM, Green DJ, Cable NT,Jones H. Exercise training improves cutaneous microvascular function in nonalcoholic fatty liver disease. Am J Physiol Endocrinol Metab 2013; 305: E50-8. DOI: https://doi.org/10.1152/ajpendo.00055.2013
Pugh CJ, Spring VS, Kemp GJ, Richardson P, Shojaee-Moradie F, Umpleby AM, Green DJ, Cable NT, Jones H,Cuthbertson DJ. Exercise training reverses endothelial dysfunction in nonalcoholic fatty liver disease. Am J Physiol Heart Circ Physiol 2014; 307: H1298-306. DOI: https://doi.org/10.1152/ajpheart.00306.2014
Shojaee-Moradie F, Cuthbertson DJ, Barrett M, Jackson NC, Herring R, Thomas EL, Bell J, Kemp GJ, Wright J,Umpleby AM. Exercise Training Reduces Liver Fat and Increases Rates of VLDL Clearance But Not VLDL Production in NAFLD. The Journal of Clinical Endocrinology & Metabolism 2016; 101: 4219-28. DOI: https://doi.org/10.1210/jc.2016-2353
Hallsworth K, Thoma C, Hollingsworth KG, Cassidy S, Anstee QM, Day CP,Trenell MI. Modified high-intensity interval training reduces liver fat and improves cardiac function in non- alcoholic fatty liver disease: a randomized controlled trial. Clin Sci (Lond) 2015; 129: 1097- 105. DOI: https://doi.org/10.1042/CS20150308
Houghton D, Thoma C, Hallsworth K, Cassidy S, Hardy T, Burt AD, Tiniakos D, Hollingsworth KG, Taylor R, Day CP, McPherson S, Anstee QM,Trenell MI. Exercise Reduces Liver Lipids and Visceral Adiposity in Patients With Nonalcoholic Steatohepatitis in a Randomized Controlled Trial. Clin Gastroenterol Hepatol. 2017; 15: 96–102.e3. DOI: https://doi.org/10.1016/j.cgh.2016.07.031
ChengS,GeJ,ZhaoC,LeS,YangY,KeD,Wu N,TanX,ZhangX,DuX,SunJ,WangR,ShiY, Borra RJH, Parkkola R, Wiklund P,Lu D. Effect of aerobic exercise and diet on liver fat in pre-diabetic patients with non-alcoholic-fatty-liver-disease: A randomized controlled trial. Sci Rep 2017; 7: 15952. DOI: https://doi.org/10.1038/s41598-017-16159-x
Smart NA, Waldron M, Ismail H, Giallauria F, Vigorito C, Cornelissen V,Dieberg G. Validation of a new tool for the assessment of study quality and reporting in exercise training studies: TESTEX. Int J Evid Based Healthc 2015; 13: 9-18. DOI: https://doi.org/10.1097/XEB.0000000000000020
Oxfeldt M, Overgaard K, Hvid LG,Dalgas U. Effects of plyometric training on jumping, sprint performance, and lower body muscle strength in healthy adults: A systematic review and meta- analyses. Scand J Med Sci Sports 2019; 29: 1453- 65. DOI: https://doi.org/10.1111/sms.13487
Review Manager (RevMan) [Computer program] v. 5.4 (The Cochrane Collaboration, 2020).
Takeshima N, Sozu T, Tajika A, Ogawa Y, Hayasaka Y,Furukawa TA. Which is more generalizable, powerful and interpretable in meta- analyses, mean difference or standardized mean difference? BMC Med Res Methodol 2014; 14: 30. DOI: https://doi.org/10.1186/1471-2288-14-30
Cohen J. Statistical Power Analysis for the Behavioral Sciences. (Routledge, 1988).
Higgins JP ,Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21: 1539-58. DOI: https://doi.org/10.1002/sim.1186
Franco I, Bianco A, Diaz MDP, Bonfiglio C, Chiloiro M, Pou SA, Becaria Coquet J, Mirizzi A, Nitti A, Campanella A, Leone CM, Caruso MG, Correale M,Osella AR. Effectiveness of two physical activity programs on non-alcoholic fatty liver disease. a randomized controlled clinical trial. Rev Fac Cien Med Univ Nac Cordoba 2019; 76: 26- 36. DOI: https://doi.org/10.31053/1853.0605.v76.n1.21638
Katsagoni CN, Papatheodoridis GV, Ioannidou P, Deutsch M, Alexopoulou A, Papadopoulos N, Papageorgiou MV, Fragopoulou E,Kontogianni MD. Improvements in clinical characteristics of patients with non-alcoholic fatty liver disease, after an intervention based on the Mediterranean lifestyle: a randomised controlled clinical trial. Br J Nutr 2018; 120: 164-75. DOI: https://doi.org/10.1017/S000711451800137X
Axley P, Kodali S, Kuo YF, Ravi S, Seay T, Parikh NM,Singal AK. Text messaging approach improves weight loss in patients with nonalcoholic fatty liver disease: A randomized study. Liver Int 2018; 38: 924-31. DOI: https://doi.org/10.1111/liv.13622
Draz RS, Serry ZMH, Rahmy AF, El Bardesi MS,Taha MM. Electroacupuncture Versus Aerobic Interval Training on Liver Functions in Patients with Nonalcoholic Fatty Liver. J Altern Complement Med 2020; 26: 51-7. DOI: https://doi.org/10.1089/acm.2019.0182
Abd El-Kader SM, Al-Shreef FM,Al-Jiffri OH. Biochemical parameters response to weight loss in patients with non-alcoholic steatohepatitis. Afr Health Sci 2016; 16: 242-9. DOI: https://doi.org/10.4314/ahs.v16i1.32
Skrypnik D, Ratajczak M, Karolkiewicz J, Mądry E, Pupek-Musialik D, Hansdorfer-Korzon R, Walkowiak J, Jakubowski H,Bogdański P. Effects of endurance and endurance-strength exercise on biochemical parameters of liver function in women with abdominal obesity. Biomed Pharmacother 2016; 80: 1-7. DOI: https://doi.org/10.1016/j.biopha.2016.02.017
Yoshimura E, Kumahara H, Tobina T, Matsuda T, Ayabe M, Kiyonaga A, Anzai K, Higaki Y,Tanaka H. Lifestyle intervention involving calorie restriction with or without aerobic exercise training improves liver fat in adults with visceral adiposity. J Obes 2014; 2014: 197216. DOI: https://doi.org/10.1155/2014/197216
Zelber-Sagi S, Buch A, Yeshua H, Vaisman N, Webb M, Harari G, Kis O, Fliss-Isakov N, Izkhakov E, Halpern Z, Santo E, Oren R,Shibolet O. Effect of resistance training on non-alcoholic fatty-liver disease a randomized-clinical trial. World J Gastroenterol 2014; 20: 4382-92. DOI: https://doi.org/10.3748/wjg.v20.i15.4382
Straznicky NE, Lambert EA, Grima MT, Eikelis N, Nestel PJ, Dawood T, Schlaich MP, Masuo K, Chopra R, Sari CI, Dixon JB, Tilbrook AJ,Lambert GW. The effects of dietary weight loss with or without exercise training on liver enzymes in obese metabolic syndrome subjects. Diabetes Obes Metab 2012; 14: 139-48. doi:10.1111/j.1463-1326.2011. 01497.x.
St George A, Bauman A, Johnston A, Farrell G, Chey T,George J. Effect of a lifestyle intervention in patients with abnormal liver enzymes and metabolic risk factors. J Gastroenterol Hepatol 2009; 24: 399-407. DOI: https://doi.org/10.1111/j.1440-1746.2008.05694.x
Promrat K, Kleiner DE, Niemeier HM, Jackvony E, Kearns M, Wands JR, Fava JL,Wing RR. Randomized controlled trial testing the effects of weight loss on nonalcoholic steatohepatitis. Hepatology 2010; 51: 121-9. DOI: https://doi.org/10.1002/hep.23276
Winn NC, Liu Y, Rector RS, Parks EJ, Ibdah JA,Kanaley JA. Energy-matched moderate and high intensity exercise training improves nonalcoholic fatty liver disease risk independent of changes in body mass or abdominal adiposity - A randomized trial. Metabolism 2018; 78: 128-40. DOI: https://doi.org/10.1016/j.metabol.2017.08.012
Garcia AMC, Veneroso CE, Soares DD, Lima AS,Correia MITD. Effect of a Physical Exercise Program on the Functional Capacity of Liver Transplant Patients. Transplantation Proceedings 2014; 46: 1807-8. DOI: https://doi.org/10.1016/j.transproceed.2014.05.023
Rachakonda V, Wills R, DeLany JP, Kershaw EE,Behari J. Differential Impact of Weight Loss on Nonalcoholic Fatty Liver Resolution in a North American Cohort with Obesity. Obesity (Silver Spring) 2017; 25: 1360-8. DOI: https://doi.org/10.1002/oby.21890
Galbreath M, Campbell, B., LaBounty, P., Bunn, J., Dove, J., Harvey, T., Hudson, G., Gutierrez, J., Levers, K., Galvan, E., Jagim, A., Greenwood, L., Cooke, M., Greenwood, M., Rasmussen, C., & Kreider, R. Effects of Adherence to a Higher Protein Diet on Weight Loss, Markers of Health, and Functional Capacity in Older Women Participating in a Resistance-Based Exercise Program. Nutrients 2018; 10: 8. DOI: https://doi.org/10.3390/nu10081070
de Piano A, de Mello MT, Sanches Pde L, da Silva PL, Campos RM, Carnier J, Corgosinho F, Foschini D, Masquio DL, Tock L, Oyama LM, do Nascimento CM, Tufik S,Damaso AR. Long-term effects of aerobic plus resistance training on the adipokines and neuropeptides in nonalcoholic fatty liver disease obese adolescents. Eur J Gastroenterol Hepatol 2012; 24: 1313-24. DOI: https://doi.org/10.1097/MEG.0b013e32835793ac
Lee S, Bacha F, Hannon T, Kuk JL, Boesch C,Arslanian S. Effects of aerobic versus resistance exercise without caloric restriction on abdominal fat, intrahepatic lipid, and insulin sensitivity in obese adolescent boys: a randomized, controlled trial. Diabetes 2012; 61: 2787-95. DOI: https://doi.org/10.2337/db12-0214
Sanchez-Munoz V, Salas-Romero R, Del Villar- Morales A, Martinez-Coria E, Pegueros-Perez A,Franco-Sanchez JG. [Decrease of liver fat content by aerobic exercise or metformin therapy in overweight or obese women]. Rev Invest Clin 2013; 65: 307-17.
Brouwers B, Schrauwen-Hinderling VB, Jelenik T, Gemmink A, Sparks LM, Havekes B, Bruls Y, Dahlmans D, Roden M, Hesselink MKC,Schrauwen P . Exercise training reduces intrahepatic lipid content in people with and people without nonalcoholic fatty liver. Am J Physiol Endocrinol Metab 2018; 314: E165-E73. DOI: https://doi.org/10.1152/ajpendo.00266.2017
Pugh CJA, Sprung VS, Jones H, Richardson P, Shojaee-Moradie F, Umpleby AM, Green DJ, Cable NT, Trenell MI, Kemp GJ,Cuthbertson DJ. Exercise-induced improvements in liver fat and endothelial function are not sustained 12 months following cessation of exercise supervision in nonalcoholic fatty liver disease. International Journal of Obesity 2016; 40: 1927-30. DOI: https://doi.org/10.1038/ijo.2016.123
Debette-Gratien M, Tabouret T, Antonini MT, Dalmay F, Carrier P, Legros R, Jacques J, Vincent F, Sautereau D, Samuel D,Loustaud-Ratti V. Personalized adapted physical activity before liver transplantation: acceptability and results. Transplantation 2015; 99: 145-50. DOI: https://doi.org/10.1097/TP.0000000000000245
Devries MC, Samjoo IA, Hamadeh MJ, Tarnopolsky MA. Effect of endurance exercise on hepatic lipid content, enzymes, and adiposity in men and women. Obesity (Silver Spring) 2008; 16: 2281-8. DOI: https://doi.org/10.1038/oby.2008.358
Yoo HJ, Hwang SY, Cho GJ, Hong HC, Choi HY, Hwang TG, Kim SM, Blüher M, Youn B-S, Baik SH,Choi KM. Association of Glypican-4 With Body Fat Distribution, Insulin Resistance, and Nonalcoholic Fatty Liver Disease. The Journal of Clinical Endocrinology & Metabolism 2013; 98: 2897-901. DOI: https://doi.org/10.1210/jc.2012-4297
Zhang HJ, Pan LL, Ma ZM, Chen Z, Huang ZF, Sun Q, Lu Y, Han CK, Lin MZ, Li XJ, Yang SY,Li XY. Long-term effect of exercise on improving fatty liver and cardiovascular risk factors in obese adults: A 1-year follow-up study. Diabetes Obes Metab 2017; 19: 284-9. DOI: https://doi.org/10.1111/dom.12809
Abdelbasset WK, Tantawy SA, Kamel DM, Alqahtani BA, Elnegamy TE, Soliman GS,Ibrahim AA. Effects of high-intensity interval and moderate-intensity continuous aerobic exercise on diabetic obese patients with nonalcoholic fatty liver disease: A comparative randomized controlled trial. Medicine (Baltimore) 2020; 99: e19471. DOI: https://doi.org/10.1097/MD.0000000000019471
Kim H, Kim M, Kojima N, Fujino K, Hosoi E, Kobayashi H, Somekawa S, Niki Y, Yamashiro Y,Yoshida H. Exercise and Nutritional Supplementation on Community-Dwelling Elderly Japanese Women With Sarcopenic Obesity: A Randomized Controlled Trial. J Am Med Dir Assoc 2016; 17: 1011-9. DOI: https://doi.org/10.1016/j.jamda.2016.06.016
Zenith L, Meena N, Ramadi A, Yavari M, Harvey A, Carbonneau M, Ma M, Abraldes JG, Paterson I, Haykowsky MJ,Tandon P. Eight weeks of exercise training increases aerobic capacity and muscle mass and reduces fatigue in patients with cirrhosis. Clin Gastroenterol Hepatol 2014; 12: 1920-6 e2. DOI: https://doi.org/10.1016/j.cgh.2014.04.016
Johnson NA, Sachinwalla T, Walton DW, Smith K, Armstrong A, Thompson MW,George J. Aerobic exercise training reduces hepatic and visceral lipids in obese individuals without weight loss. Hepatology 2009; 50: 1105-12. DOI: https://doi.org/10.1002/hep.23129
Kim BJ, Ahn SH, Lee SH, Hong S, Hamrick MW, Isales CM,Koh JM. Lower hand grip strength in older adults with non-alcoholic fatty liver disease: a nationwide population-based study. Aging (Albany NY) 2019; 11: 4547–60. DOI: https://doi.org/10.18632/aging.102068
Hawley JA, Hargreaves M, Joyner MJ,Zierath JR. Integrative biology of exercise. Cell 2014; 159: 738-49. DOI: https://doi.org/10.1016/j.cell.2014.10.029
Liu TC, Liu G, Hu SJ, Zhu L, Yang XB,Zhang QG. Quantitative Biology of Exercise-Induced Signal Transduction Pathways. Adv Exp Med Biol 2017; 977: 419-24. DOI: https://doi.org/10.1007/978-3-319-55231-6_54
Francaux M,Deldicque L. Exercise and the control of muscle mass in human. Pflugers Arch 2019; 471: 397-411. DOI: https://doi.org/10.1007/s00424-018-2217-x
Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM,Ferrucci L. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol (1985) 2003; 95: 1851-60. DOI: https://doi.org/10.1152/japplphysiol.00246.2003
Milani RV, Lavie CJ, Mehra MR,Ventura HO. Understanding the basics of cardiopulmonary exercise testing. Mayo Clin Proc 2006; 81: 1603- 11. DOI: https://doi.org/10.4065/81.12.1603
Weisman IM, Weisman IM, Marciniuk D, Martinez FJ, Sciurba F, Sue D,Sietsema K. ATS/ACCP Statement on Cardiopulmonary Exercise Testing. American Journal of Respiratory and Critical Care Medicine 2003; 167: 211-77. DOI: https://doi.org/10.1164/ajrccm.167.10.952
Marchesini G, Day CP, Dufour JF, Canbay A, Nobili V, Ratziu V,Mathus-Vliegen L. EASL- EASD-EASO Clinical Practice Guidelines for the Management of Non-Alcoholic Fatty Liver Disease. Obesity Facts 2016; 9: 56-90.
Lee I, Kim J,Kang H. Estimated Cardiorespiratory Fitness Attenuates the Impacts of Sarcopenia and Obesity on Non-Alcoholic Fatty Liver in Korean Adults. Int J Environ Res Public Health 2020; 17: 3902. DOI: https://doi.org/10.3390/ijerph17113902
Hughes DC, Ellefsen S,Baar K. Adaptations to Endurance and Strength Training. LID - 10.1101/cshperspect.a029769 [doi] LID - a029769. Cold Spring Harb Perspect Med 2018; 8. DOI: https://doi.org/10.1101/cshperspect.a029769
McGee SL,Hargreaves M. Exercise adaptations: molecular mechanisms and potential targets for therapeutic benefit. Nat Rev Endocrinol 2020; 16: 495-505. DOI: https://doi.org/10.1038/s41574-020-0377-1
Lo MS, Lin LL, Yao WJ,Ma MC. Training and detraining effects of the resistance vs. endurance program on body composition, body size, and physical performance in young men. J Strength Cond Res 2011; 25: 2246-54. DOI: https://doi.org/10.1519/JSC.0b013e3181e8a4be
Nolan PB, Keeling SM, Robitaille CA, Buchanan CA,Dalleck LC. The Effect of Detraining after a Period of Training on Cardiometabolic Health in Previously Sedentary Individuals. Int J Environ Res Public Health 2018; 15: 2303. DOI: https://doi.org/10.3390/ijerph15102303
Brouwers B, Hesselink MK, Schrauwen P ,Schrauwen-Hinderling VB. Effects of exercise training on intrahepatic lipid content in humans. Diabetologia 2016; 59: 2068–79. DOI: https://doi.org/10.1007/s00125-016-4037-x
van der Windt DJ, Sud V, Zhang H, Tsung A,Huang H. The Effects of Physical Exercise on Fatty Liver Disease. Gene Expr 2018; 18: 89-101. DOI: https://doi.org/10.3727/105221617X15124844266408
Dunn MA, Rogal SS, Duarte-Rojo A,Lai JC. Physical Function, Physical Activity, and Quality of Life After Liver Transplantation. Liver Transpl 2020; 26: 702-8. DOI: https://doi.org/10.1002/lt.25742
Phu S, Kirk B, Bani Hassan E, Vogrin S, Zanker J, Bernardo S,Duque G. The diagnostic value of the Short Physical Performance Battery for sarcopenia. BMC Geriatr 2020; 20: 242. DOI: https://doi.org/10.1186/s12877-020-01642-4
Lai JC, Feng S, Terrault NA, Lizaola B, Hayssen H,Covinsky K. Frailty predicts waitlist mortality in liver transplant candidates. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2014; 14: 1870-9. DOI: https://doi.org/10.1111/ajt.12762
Wang CW, Feng S, Covinsky KE, Hayssen H, Zhou LQ, Yeh BM,Lai JC. A Comparison of Muscle Function, Mass, and Quality in Liver Transplant Candidates: Results From the Functional Assessment in Liver Transplantation Study. Transplantation 2016; 100: 1692-8. DOI: https://doi.org/10.1097/TP.0000000000001232
European Association for the Study of the Liver. Electronic address eee,European Association for the Study of the L. EASL Clinical Practice Guidelines on nutrition in chronic liver disease. J Hepatol 2019; 70: 172-93.
Naseer M, Turse EP, Syed A, Dailey FE, Zatreh M,Tahan V. Interventions to improve sarcopenia in cirrhosis: A systematic review. World J Clin Cases 2019; 7: 156-70. DOI: https://doi.org/10.12998/wjcc.v7.i2.156
Aamann L, Dam G, Borre M, Drljevic-Nielsen A, Overgaard K, Andersen H, Vilstrup H,Aagaard NK. Resistance Training Increases Muscle Strength and Muscle Size in Patients With Liver Cirrhosis. Clin Gastroenterol Hepatol 2019; 18: 1179-87.e6. DOI: https://doi.org/10.1016/j.cgh.2019.07.058
Giallauria F, Cittadini A, Smart NA,Vigorito C. Resistance training and sarcopenia. Monaldi Arch Chest Dis 2016; 84: 738. DOI: https://doi.org/10.4081/monaldi.2015.738
Csapo R,Alegre LM. Effects of resistance training with moderate vs heavy loads on muscle mass and strength in the elderly: A meta-analysis. Scand J Med Sci Sports 2016; 26: 995-1006. DOI: https://doi.org/10.1111/sms.12536
Wackerhage H, Schoenfeld BJ, Hamilton DL, Lehti M,Hulmi JJ. Stimuli and sensors that initiate skeletal muscle hypertrophy following resistance exercise. J Appl Physiol (1985) 2019; 126: 30-43. DOI: https://doi.org/10.1152/japplphysiol.00685.2018
Thompson PD, Arena R, Riebe D, Pescatello LS,American College of Sports M. ACSM's new preparticipation health screening recommendations from ACSM's guidelines for exercise testing and prescription, ninth edition. Curr Sports Med Rep 2013; 12: 215-7. DOI: https://doi.org/10.1249/JSR.0b013e31829a68cf
Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA,Rennie MJ. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 2008; 586: 3701-17. DOI: https://doi.org/10.1113/jphysiol.2008.153916

How to Cite

Gonzalez, A., Valero-Breton, M., Huerta-Salgado, C., Achiardi, O., Simon, F., & Cabello-Verrugio, C. (2021). Impact of exercise training on the sarcopenia criteria in non-alcoholic fatty liver disease: a systematic review and meta-analysis. European Journal of Translational Myology, 31(1). https://doi.org/10.4081/ejtm.2021.9630

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